Cited by 23Viral gastroenteritis research and epidemiologyAdvanced Electron Microscopy Techniques and ApplicationsEnzyme Structure and Function

Antigenic and Cryo-Electron Microscopy Structure Analysis of a Chimeric Sapovirus Capsid

Open access
Miyazaki, Naoyuki, Taylor, David W., Hansman, Grant S., Murata, Kazuyoshi·2016·Journal of Virology

Abstract

The capsid protein (VP1) of all caliciviruses forms an icosahedral particle with two principal domains, shell (S) and protruding (P) domains, which are connected via a flexible hinge region. The S domain forms a scaffold surrounding the nucleic acid, while the P domains form a homodimer that interacts with receptors. The P domain is further subdivided into two subdomains, termed P1 and P2. The P2 subdomain is likely an insertion in the P1 subdomain; consequently, the P domain is divided into the P1-1, P2, and P1-2 subdomains. In order to investigate capsid antigenicity, N-terminal (N-term)/S/P1-1 and P2/P1-2 were switched between two sapovirus genotypes GI.1 and GI.5. The chimeric VP1 constructs were expressed in insect cells and were shown to self-assemble into virus-like particles (VLPs) morphologically similar to the parental VLPs. Interestingly, the chimeric VLPs had higher levels of cross-reactivities to heterogeneous antisera than the parental VLPs. In order to better understand the antigenicity from a structural perspective, we determined an intermediate-resolution (8.5-Å) cryo-electron microscopy (cryo-EM) structure of a chimeric VLP and developed a VP1 homology model. The cryo-EM structure revealed that the P domain dimers were raised slightly (∼5 Å) above the S domain. The VP1 homology model allowed us predict the S domain (67–229) and P1-1 (229–280), P2 (281–447), and P1-2 (448–567) subdomains. Our results suggested that the raised P dimers might expose immunoreactive S/P1-1 subdomain epitopes. Consequently, the higher levels of cross-reactivities with the chimeric VLPs resulted from a combination of GI.1 and GI.5 epitopes. IMPORTANCE We developed sapovirus chimeric VP1 constructs and produced the chimeric VLPs in insect cells. We found that both chimeric VLPs had a higher level of cross-reactivity against heterogeneous VLP antisera than the parental VLPs. The cryo-EM structure of one chimeric VLP (Yokote/Mc114) was solved to 8.5-Å resolution. A homology model of the VP1 indicated for the first time the putative S and P (P1-1, P2, and P1-2) domains. The overall structure of Yokote/Mc114 contained features common among other caliciviruses. We showed that the P2 subdomain was mainly involved in the homodimeric interface, whereas a large gap between the P1 subdomains had fewer interactions.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/jvi.02916-15

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Expression of a recombinant form of the major capsid protein is sufficient for the assembly of virus-like particles (VLPs), which exhibit the same morphology as virions.

    “As is the case for many members of the Caliciviridae, expression of a recombinant form of the major capsid protein is sufficient for the assembly of virus-like particles (VLPs), which exhibit the same morphology as virions [26–29].”

    From Vesivirus 2117 capsids more closely resemble sapovirus and lagovirus particles than other known vesivirus structures (2017) · cites this paper as [28]

    The Abstract (page unavailable) says that recombinant chimeric VP1 self-assembled into VLPs. It describes those VLPs as morphologically similar to parental VLPs, not as having the same morphology as virions. The Results and Discussion report structural similarities to a vesivirus virion, but do not establish the broader morphology claim. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 26

  1. Hansman GS, Jiang XJ, Green KY. 2010. Caliciviruses: molecular and cellular virology. Caister Academic Press, Norfolk, United Kingdom.
  2. Hansman GS, Oka T, Sakon N, Takeda N. 2007. Antigenic diversity of human sapoviruses. Emerg Infect Dis 13:1519 -1525. http://dx.doi.org/10 .3201/eid1310.070402. · DOI
  3. Hansman GS, Oka T, Katayama K, Takeda N. 2007. Human sapovi- ruses: genetic diversity, recombination, and classification. Rev Med Virol 17:133-141. http://dx.doi.org/10.1002/rmv.533. · DOI
  4. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286:287-290. http://dx.doi.org/10.1126/science.286.5438.287. · DOI
  5. Chen R, Neill JD, Prasad BV. 2003. Crystallization and preliminary crystallographic analysis of San Miguel sea lion virus: an animal calicivi- rus. J Struct Biol 141:143-148. http://dx.doi.org/10.1016/S1047-8477 (02)00583-X. · DOI · Paper page
  6. Schulten K, Zheng D, Pang H, Sun F. 2013. Atomic model of rabbit hemorrhagic disease virus by cryo-electron microscopy and crystallogra- phy. PLoS Pathog 9:e1003132. http://dx.doi.org/10.1371/journal.ppat .1003132. · DOI
  7. Leuthold MM, Dalton KP, Hansman GS. 2015. Structural analysis of a rabbit hemorrhagic disease virus binding to histo-blood group antigens. J Virol 89:2378 -2387. http://dx.doi.org/10.1128/JVI.02832-14. · DOI
  8. Bhella D, Goodfellow IG. 2011. The cryo-electron microscopy structure of feline calicivirus bound to junctional adhesion molecule A at 9-ang- strom resolution reveals receptor-induced flexibility and two distinct con- formational changes in the capsid protein VP1. J Virol 85:11381-11390. http://dx.doi.org/10.1128/JVI.05621-11. · DOI · Paper page
  9. Cao S, Lou Z, Tan M, Chen Y, Liu Y, Zhang Z, Zhang XC, Jiang X, Li X, Rao Z. 2007. Structural basis for the recognition of blood group tri- saccharides by norovirus. J Virol 81:5949 -5957. http://dx.doi.org/10.1128 /JVI.00219-07. · DOI
  10. Chen R, Neill JD, Noel JS, Hutson AM, Glass RI, Estes MK, Prasad BV. 2004. Inter-and intragenus structural variations in caliciviruses and their functional implications. J Virol 78:6469 -6479. http://dx.doi.org/10.1128 /JVI.78.12.6469-6479.2004. · DOI · Paper page
  11. Chen R, Neill JD, Estes MK, Prasad BV. 2006. X-ray structure of a native calicivirus: structural insights into antigenic diversity and host specificity. Proc Natl Acad Sci U S A 103:8048 -8053. http://dx.doi.org/10.1073/pnas .0600421103. · DOI · Paper page
  12. Hansman GS, Taylor DW, McLellan JS, Smith TJ, Georgiev I, Tame JR, Park SY, Yamazaki M, Gondaira F, Miki M, Katayama K, Murata K, Kwong PD. 2012. Structural basis for broad detection of genogroup II noroviruses by a monoclonal antibody that binds to a site occluded in the viral particle. J Virol 86:3635-3646. http://dx.doi.org/10.1128 /JVI.06868-11. · DOI
  13. Hansman GS, Saito H, Shibata C, Ishizuka S, Oseto M, Oka T, Takeda N. 2007. Outbreak of gastroenteritis due to sapovirus. J Clin Microbiol 45:1347-1349. http://dx.doi.org/10.1128/JCM.01854-06. · DOI
  14. Hansman GS, Natori K, Oka T, Ogawa S, Tanaka K, Nagata N, Ushi- jima H, Takeda N, Katayama K. 2005. Cross-reactivity among sapovirus recombinant capsid proteins. Arch Virol 150:21-36. http://dx.doi.org/10 .1007/s00705-004-0406-8. · DOI
  15. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for electron micros- copy. J Struct Biol 157:38 -46. http://dx.doi.org/10.1016/j.jsb.2006.05.009. · DOI
  16. Rosenthal PB, Henderson R. 2003. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333:721-745. http://dx.doi.org/10.1016/j.jmb .2003.07.013. · DOI · Paper page
  17. Sali A. 1995. Comparative protein modeling by satisfaction of spatial restraints. Mol Med Today 1:270 -277. http://dx.doi.org/10.1016/S1357 -4310(95)91170-7. · DOI
  18. Pei J, Tang M, Grishin NV. 2008. PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36:W30 -W34. http://dx.doi.org/10.1093/nar/gkn322. · DOI
  19. Pei J, Kim BH, Grishin NV. 2008. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res 36:2295- 2300. http://dx.doi.org/10.1093/nar/gkn072. · DOI
  20. Topf M, Lasker K, Webb B, Wolfson H, Chiu W, Sali A. 2008. Protein structure fitting and refinement guided by cryo-EM density. Structure 16:295-307. http://dx.doi.org/10.1016/j.str.2007.11.016. · DOI
  21. Debbink K, Lindesmith LC, Donaldson EF, Swanstrom J, Baric RS. 2014. Chimeric GII.4 norovirus virus-like-particle-based vaccines induce broadly blocking immune responses. J Virol 88:7256 -7266. http://dx.doi .org/10.1128/JVI.00785-14. · DOI
  22. Kleywegt GJ, Zou J-Y, Kjeldgaard. M, Jones TA. 2001. Crystallography of biological macromolecules. Around O, Chapter 17.1, p 353-356, 366 - 367. In Rossmann MG, Arnold E (ed), International tables for crystallog- raphy, vol F. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  23. Katpally U, Voss NR, Cavazza T, Taube S, Rubin JR, Young VL, Stuckey J, Ward VK, Virgin HW, IV, Wobus CE, Smith TJ. 2010. High-resolution cryo-electron microscopy structures of murine norovi- rus 1 and rabbit hemorrhagic disease virus reveal marked flexibility in the receptor binding domains. J Virol 84:5836 -5841. http://dx.doi.org/10 .1128/JVI.00314-10. · DOI · Paper page
  24. Parra GI, Azure J, Fischer R, Bok K, Sandoval-Jaime C, Sosnovtsev SV, Sander P, Green KY. 2013. Identification of a broadly cross-reactive epitope in the inner shell of the norovirus capsid. PLoS One 8:e67592. http://dx.doi.org/10.1371/journal.pone.0067592. · DOI
  25. Parker TD, Kitamoto N, Tanaka T, Hutson AM, Estes MK. 2005. Identification of genogroup I and genogroup II broadly reactive epitopes on the norovirus capsid. J Virol 79:7402-7409. http://dx.doi.org/10.1128 /JVI.79.12.7402-7409.2005. · DOI
  26. Shiota T, Okame M, Takanashi S, Khamrin P, Takagi M, Satou K, Masuoka Y, Yagyu F, Shimizu Y, Kohno H, Mizuguchi M, Okitsu S, Ushijima H. 2007. Characterization of a broadly reactive monoclonal antibody against norovirus genogroups I and II: recognition of a novel conformational epitope. J Virol 81:12298 -12306. http://dx.doi.org/10 .1128/JVI.00891-07. · DOI

Cited by

Sorted by citations

Authors
Miyazaki, N., Taylor, D. W., Hansman, G. S., & Murata, K.
Affiliations
  • National Institute for Physiological Sciences (JP)
  • Yale University (US)
  • German Cancer Research Center (DE)
Venue
Journal of Virology
Published
2016-03
Volume
90
Issue
5
Pages
2664-2675
ISSN
  • 0022-538X (ISSN-L)
  • 1098-5514
OpenAlex
W2208906706
Cited by
23
References
1
Citations by year
2026: 3 · 2025: 3 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 2 · 2017: 1 · 2016: 1
FWCI
0.52
Type
journal article
Language
en
Open access
Locations
  • Journal of Virology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Griffith Research Online (submittedVersion)
Funders
Japan Society for the Promotion of Science (25251009)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Viral gastroenteritis research and epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
Keywords
sapovirus, calicivirus, VP1 capsid protein, virus-like particles, antigenic determinants, cross-reactivity, cryo-EM structure, P domain, S domain, insect cell expression, vaccine candidate, epitope mapping, receptor binding domain
MeSH terms
Amino Acid Sequence, Antibodies, Viral, Antigens, Viral, Cross Reactions, Molecular Sequence Data, Recombinant Proteins, Recombination, Genetic, Cryoelectron Microscopy, Virosomes, Sapovirus, Capsid Proteins, Protein Multimerization

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review